Abstract
There is growing interest in understanding the role that plant–soil feedbacks (PSFs) may play in invasion resistance. However, recent studies have shown that there is great uncertainty in explaining community patterns by PSF studies regarding invasions. This uncertainty may be partly because soils used for PSF studies are usually collected from open areas rather than natural communities, thus ignoring the effects of community contexts that may specifically influence the soil feedbacks of community residents to invaders. We performed a two-phase pot experiment to study the soil feedback initiated by ten co-occurring native and exotic species to a forest invader, Phytolacca americana, and the experiments were performed in forest soil and open area soil. The context-dependent mechanisms were further explored by studying different components of PSF. The results showed that natives and exotics had positive and negative effects on P. americana in the open area soil, respectively, but both had negative effects in the forest soil. Nutrient limitation was more important for the PSF in open area soil, whereas biotic factors were likely the primary mechanisms explaining the PSF in forest soil. Additionally, the litter-mediated allelopathy of dominant Quercus acutissima caused the strongest inhibition of the invader. These results suggest that native species can effectively resist invasion by producing negative PSF depending on the community context. Evidence that exotic species promote invasion through positive PSFs was not obtained. This study provided preliminary insights into the possibility of bridging PSF studies and community patterns.
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References
Aldorfova A, Knobova P, Munzbergova Z (2020) Plant–soil feedback contributes to predicting plant invasiveness of 68 alien plant species differing in invasive status. Oikos 129:1257–1270. https://doi.org/10.1111/oik.07186
Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 6:1–48. https://doi.org/10.18637/jss.v067.i01
Bennett JA, Klironomos J (2019) Mechanisms of plant–soil feedback: interactions among biotic and abiotic drivers. New Phytol 222:91–96. https://doi.org/10.1111/nph.15603
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. https://doi.org/10.1126/science.aai8212
Bradley BA, Blumenthal DM, Wilcove DS, Ziska LH (2010) Predicting plant invasions in an era of global change. Trends Ecol Evol 25:310–318. https://doi.org/10.1016/j.tree.2009.12.003
Brinkman EP, Van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073. https://doi.org/10.1111/j.1365-2745.2010.01695.x
Bufford JL, Lurie MH, Daehler CC (2016) Biotic resistance to tropical ornamental invasion. J Ecol 104:518–530. https://doi.org/10.1111/1365-2745.12534
Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055. https://doi.org/10.1890/07-0370.1
Catford JA, Smith AL, Wragg PD, Clark AT, Kosmala M, Cavender-Bares J et al (2019) Traits linked with species invasiveness and community invasibility vary with time, stage and indicator of invasion in a long-term grassland experiment. Ecol Lett 22:593–604. https://doi.org/10.1111/ele.13220
Chen BM, Peng SL, Ni GY (2009) Effects of the invasive plant Mikania micrantha H.B.K. on soil nitrogen availability through allelopathy in South China. Biol Invasions 11:1291–1299. https://doi.org/10.1007/s10530-008-9336-9
Chen PD, Hou YP, Zhuge YH, Wei W, Huang QQ (2019a) The effects of soils from different forest types on the growth of the invasive plant Phytolacca americana. Forests 10:492. https://doi.org/10.3390/f10060492
Chen PD, Hou YP, Wei W, Lu X, Han LP, Ni GY (2019b) Allelopathic effects of seven common species on the growth of alien invasive plant Phytolacca americana. Allelopathy J 47:195–207. https://doi.org/10.26651/allelo.j/2019-47-2-1231
Courchamp F, Fournier A, Bellard C, Bertelsmeier C, Bonnaud E, Jeschke JM, Russell JC (2017) Invasion biology: specific problems and possible solutions. Trends Ecol Evol 32:13–22. https://doi.org/10.1016/j.tree.2016.11.001
Crawford KM, Knight TM (2017) Competition overwhelms the positive plant-soil feedback generated by an invasive plant. Oecologia 183:211–220. https://doi.org/10.1007/s00442-016-3759-2
Crawford KM, Bauer JT, Comita LS, Eppinga MB, Johnson DJ, Mangan SA et al (2019) When and where plant–soil feedback may promote plant coexistence: a meta-analysis. Ecol Lett 22:1274–1284. https://doi.org/10.1111/ele.13278
Cummings JA, Parker IM, Gilbert GS (2012) Allelopathy: a tool for weed management in forest restoration. Plant Ecol 213:1975–1989. https://doi.org/10.1007/s11258-012-0154-x
DA Inderjit W, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655–662. https://doi.org/10.1016/j.tree.2011.08.003
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
Del Fabbro C, Prati D (2015) The relative importance of immediate allelopathy and allelopathic legacy in invasive plant species. Basic Appl Ecol 16:28–35. https://doi.org/10.1016/j.baae.2014.10.007
Elgersma KJ, Yu S, Vor T, Ehrenfeld JG (2012) Microbial-mediated feedbacks of leaf litter on invasive plant growth and interspecific competition. Plant Soil 356:341–355. https://doi.org/10.1007/s11104-011-1117-z
Forero LE, Grenzerl J, Heinze J, Schittko C, Kulmatiski A (2019) Greenhouse- and field-measured plant–soil feedbacks are not correlated. Front Environ Sci 7:8. https://doi.org/10.3389/fenvs.2019.00184
Fu JP, Li CR, Xu JW, Cheng WL, Song RF, Liu Y (2012) Prevention and control of invaded plant Phytolacca americana in sandy coastal shelter forests. Chin J Appl Ecol 23:991–997 ((in Chinese with English abstract))
Grove S, Haubensak KA, Parker IM (2012) Direct and indirect effects of allelopathy in the soil legacy of an exotic plant invasion. Plant Ecol 213:1869–1882. https://doi.org/10.1007/s11258-012-0079-4
Hou YP, Peng SL, Chen BM, Ni GY (2011) Inhibition of an invasive plant (Mikania micrantha H.B.K.) by soils of three different forests in lower subtropical China. Biol Invasions 13:381–391. https://doi.org/10.1007/s10530-010-9830-8
Huang W, Ding J (2016) Effects of generalist herbivory on resistance and resource allocation by the invasive plant, Phytolacca americana. Insect Sci 23:191–199. https://doi.org/10.1111/1744-7917.12244
Huangfu CH, Hui DF, Qi XX, Li KL (2019) Plant interactions modulate root litter decomposition and negative plant–soil feedback with an invasive plant. Plant Soil 437:179–194. https://doi.org/10.1007/s11104-019-03973-7
Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. Isme J 3:442–453. https://doi.org/10.1038/ismej.2008.127
Kaisermann A, de Vries FT, Griffiths RI, Bardgett RD (2017) Legacy effects of drought on plant–soil feedbacks and plant-plant interactions. New Phytol 215:1413–1424. https://doi.org/10.1111/nph.14661
Kong CH, Zhang SZ, Li YH, Xia ZC, Yang XF, Meiners SJ, Wang P (2018) Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals. Nat Commun. https://doi.org/10.1038/s41467-018-06429-1
Kulmatiski A (2019) Plant–soil feedbacks predict native but not non-native plant community composition: a 7-year common-garden experiment. Front Ecol Evol 7:326. https://doi.org/10.3389/fevo.2019.00326
Kulmatiski A, Beard KH (2011) Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure. Soil Biol Biochem 43:823–830. https://doi.org/10.1016/j.soilbio.2010.12.018
Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. https://doi.org/10.1111/j.1461-0248.2008.01209.x
Kulmatiski A, Beard KH, Norton JM, Heavilin JE, Forero LE, Grenzer J (2017) Live long and prosper: plant–soil feedback, lifespan, and landscape abundance covary. Ecology 98:3063–3073. https://doi.org/10.1002/ecy.2011
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. https://doi.org/10.1111/j.1461-0248.2004.00657.x
Li XG, Ding CF, Hua K, Zhang TL, Zhang YN, Zhao L et al (2014) Soil sickness of peanuts is attributable to modifications in soil microbes induced by peanut root exudates rather than to direct allelopathy. Soil Biol Biochem 78:149–159. https://doi.org/10.1016/j.soilbio.2014.07.019
Li YP, Feng YL, Kang ZL, Zheng YL, Zhang JL, Chen YJ (2017) Changes in soil microbial communities due to biological invasions can reduce allelopathic effects. J Appl Ecol 54:1281–1290. https://doi.org/10.1111/1365-2664.12878
Liu S, Qin F, Yu S (2018) Eucalyptus urophylla root-associated fungi can counteract the negative influence of phenolic acid allelochemicals. Appl Soil Ecol 127:1–7. https://doi.org/10.1016/j.apsoil.2018.02.028
Macias FA, Mejias FJR, Molinillo JMG (2019) Recent advances in allelopathy for weed control: from knowledge to applications. Pest Manag Sci 75:2413–2436. https://doi.org/10.1002/ps.5355
Medina-Villar S, Rodríguez-Echeverría S, Lorenzo P, Alonso A, Pérez-Corona E, Castro-Díez P (2016) Impacts of the alien trees Ailanthus altissima (Mill.) Swingle and Robinia pseudoacacia L. on soil nutrients and microbial communities. Soil Biol Biochem 96:65–73. https://doi.org/10.1016/j.soilbio.2016.01.015
Meiners SJ, Phipps KK, Pendergast TH, Canam T, Carson WP (2017) Soil microbial communities alter leaf chemistry and influence allelopathic potential among coexisting plant species. Oecologia 183:1155–1165. https://doi.org/10.1007/s00442-017-3833-4
Ning L, Yu FH, van Kleunen M (2016) Allelopathy of a native grassland community as a potential mechanism of resistance against invasion by introduced plants. Biol Invasions 18:3481–3493. https://doi.org/10.1007/s10530-016-1239-6
Oksanen L, Sammul M, Magi M (2006) On the indices of plant-plant competition and their pitfalls. Oikos 112:149–155. https://doi.org/10.1111/j.0030-1299.2006.13379.x
Orozco-Aceves M, Standish RJ, Tibbett M (2015) Soil conditioning and plant–soil feedbacks in a modified forest ecosystem are soil-context dependent. Plant Soil 390:183–194. https://doi.org/10.1007/s11104-015-2390-z
Pearson DE, Ortega YK, Villarreal D, Lekberg Y, Cock MC, Eren O, Hierro JL (2018) The fluctuating resource hypothesis explains invasibility, but not exotic advantage following disturbance. Ecology 99:1296–1305. https://doi.org/10.1002/ecy.2235
Perkins LB, Nowak RS (2013) Native and non-native grasses generate common types of plant–soil feedbacks by altering soil nutrients and microbial communities. Oikos 122:199–208. https://doi.org/10.1111/j.1600-0706.2012.20592.x
Ricciardi A, Blackburn TM, Carlton JT, Dick JTA, Hulme PE, Iacarella JC et al (2017) Invasion science: a horizon scan of emerging challenges and opportunities. Trends Ecol Evol 32:464–474. https://doi.org/10.1016/j.tree.2017.03.007
Salminen JP, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711. https://doi.org/10.1023/b:joec.0000042396.40756.b7
Schittko C, Runge C, Strupp M, Wolff S, Wurst S (2016) No evidence that plant–soil feedback effects of native and invasive plant species under glasshouse conditions are reflected in the field. J Ecol 104:1243–1249. https://doi.org/10.1111/1365-2745.12603
Smith-Ramesh LM (2018) Predators in the plant–soil feedback loop: aboveground plant-associated predators may alter the outcome of plant–soil interactions. Ecol Lett 21:646–654. https://doi.org/10.1111/ele.12931
Smith-Ramesh LM, Reynolds HL (2017) The next frontier of plant–soil feedback research: unraveling context dependence across biotic and abiotic gradients. J Veg Sci 28:484–494. https://doi.org/10.1111/jvs.12519
Suding KN, Stanley Harpole W, Fukami T, Kulmatiski A, MacDougall AS, Stein C et al (2013) Consequences of plant–soil feedbacks in invasion. J Ecol 101:298–308. https://doi.org/10.1111/1365-2745.12057
Troelstra SR, Wagenaar R, Smant W, Peters BAM (2001) Interpretation of bioassays in the study of interactions between soil organisms and plants: involvement of nutrient factors. New Phytol 150:697–706. https://doi.org/10.1046/j.1469-8137.2001.00133.x
van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T et al (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. https://doi.org/10.1111/1365-2745.12054
Veen GF, Fry EL, ten Hooven FC, Kardol P, Morrien E, De Long JR (2019) The role of plant litter in driving plant–soil feedbacks. Front Environ Sci 7:10. https://doi.org/10.3389/fenvs.2019.00168
Wei W, Zhu P, Chen P, Huang Q, Bai X, Ni G, Hou Y (2020) Mixed evidence for plant–soil feedbacks in forest invasions. Oecologia. https://doi.org/10.1007/s00442-020-04703-y
Xiao L, Hervé MR, Carrillo J, Ding J, Huang W (2019) Latitudinal trends in growth, reproduction and defense of an invasive plant. Biol Invasions 21:189–201. https://doi.org/10.1007/s10530-018-1816-y
Yannelli FA, Koch C, Jeschke JM, Kollmann J (2017) Limiting similarity and Darwin’s naturalization hypothesis: understanding the drivers of biotic resistance against invasive plant species. Oecologia 183:775–784. https://doi.org/10.1007/s00442-016-3798-8
Ye XQ, Yan YN, Wu M, Yu FH (2019) High capacity of nutrient accumulation by invasive Solidago canadensis in a coastal grassland. Front Plant Sci 10:575. https://doi.org/10.3389/fpls.2019.00575
Zhang J, Bai X, Hou Y, Dong Z, Bu Q (2016) Comparison on the competitiveness of the invaded pokeweed with its accompanying species in the coastal protection forest of Shandong Peninsula. Sci Silvae Sin 52:23–29 ((in Chinese with English abstract))
Zhang P, Li B, Wu JH, Hu SJ (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol Lett 22:200–210. https://doi.org/10.1111/ele.13181
Zhang HY, Goncalves P, Copeland E, Qi SS, Dai ZC, Li GL et al (2020a) Invasion by the weed Conyza canadensis alters soil nutrient supply and shifts microbiota structure. Soil Biol Biochem 143:107739. https://doi.org/10.1016/j.soilbio.2020.107739
Zhang ZJ, Liu YJ, Brunel C, van Kleunen M (2020b) Evidence for Elton’s diversity-invasibility hypothesis from belowground. Ecology. https://doi.org/10.1002/ecy.3187
Zhang ZJ, Liu YJ, Yuan L, Weber E, van Kleunen M (2020c) Effect of allelopathy on plant performance: a meta-analysis. Ecol Lett 24:348–362. https://doi.org/10.1111/ele.13627
Zhao H, Peng S, Chen Z, Wu Z, Zhou G, Wang X, Qiu Z (2011) Abscisic acid in soil facilitates community succession in three forests in China. J Chem Ecol 37:785–793. https://doi.org/10.1007/s10886-011-9970-z
Zhou B, Yan X, Xiao Y, Zhang Z, Xiaohong LI (2013) Traits of reproductive biology associated with invasiveness in alien invasive plant Phytolacca americana. Ecol Environ Sci 22:567–574 ((in Chinese with English abstract))
Acknowledgements
We would like to thank Dr. Fangfang Huang from Gangdong Academy of Forestry, Dr. Enjian Chen from Sun Yat-sen University, and Dr. Leiyi Chen from Chinese Academy of Sciences for comments on this manuscript. This study was funded by the National Natural Science Foundation of China (31770581; 31300465) and the Shandong Province Higher Educational Science and Technology Program (J17KA128). We thank the editors and the anonymous referees for the valuable comments on improvements of the manuscript.
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PC, QH and YH conceived and designed the study. PC, YZ and CL performed the experiments and collected the data. PC and PZ carried out the data analysis. PC led the writing of the manuscript. QH and YH reviewed and edited the manuscript. All authors participated in data interpretation and revised the manuscript.
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Communicated by Sarah M. Emery.
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Chen, P., Huang, Q., Zhuge, Y. et al. The effects of plant–soil feedback on invasion resistance are soil context dependent. Oecologia 197, 213–222 (2021). https://doi.org/10.1007/s00442-021-05004-8
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DOI: https://doi.org/10.1007/s00442-021-05004-8